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Involvement of the Left Supramarginal Gyrus in Manipulation Judgment Tasks: Contributions to Theories of Tool Use

Published online by Cambridge University Press:  19 June 2017

Mathieu Lesourd ,
François Osiurak ,
Jordan Navarro  and
Emanuelle Reynaud
Mathieu Lesourd*
Affiliation:
Laboratoire d’Etude des Mécanismes Cognitifs (EA 3082), Université de Lyon, France
François Osiurak
Affiliation:
Laboratoire d’Etude des Mécanismes Cognitifs (EA 3082), Université de Lyon, France Institut Universitaire de France, Paris, France
Jordan Navarro
Affiliation:
Laboratoire d’Etude des Mécanismes Cognitifs (EA 3082), Université de Lyon, France
Emanuelle Reynaud
Affiliation:
Laboratoire d’Etude des Mécanismes Cognitifs (EA 3082), Université de Lyon, France
*
Correspondence and reprint requests to: Mathieu Lesourd, Laboratoire d’Etude des Mécanismes Cognitifs (EA 3082), Institut de Psychologie, 5, avenue Pierre Mendès-France, 69676 BronCedex, France. E-mail: mathieu.lesourd@chu-lyon.fr
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Abstract

Objectives: Two theories of tool use, namely the gesture engram and the technical reasoning theories, make distinct predictions about the involvement of the left inferior parietal lobe (IPL) in manipulation judgement tasks. The objective here is to test these alternative predictions based on previous studies on manipulation judgment tasks using transcranial magnetic stimulations (TMS) targeting the left supramarginal gyrus (SMG). Methods: We review recent TMS studies on manipulation judgement tasks and confront these data with predictions made by both tool use theories. Results: The left SMG is a highly intertwined region, organized following several functionally distinct areas and TMS may have disrupted a cortical network involved in the ability to use tools rather than only one functional area supporting manipulation knowledge. Moreover, manipulation judgement tasks may be impaired following virtual lesions outside the IPL. Conclusions: These data are more in line with the technical reasoning hypothesis, which assumes that the left IPL does not store manipulation knowledge per se. (JINS, 2017, 23, 685–691)

Keywords

TMSTool useGesture engram theoryTechnical reasoning theoryInferior parietal lobeApraxia
Type
Short Reviews
Information
Journal of the International Neuropsychological Society , Volume 23 , Issue 8 , September 2017 , pp. 685 - 691
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

REFERENCES

Andres, M., Pelgrims, B., & Olivier, E. (2013). Distinct contribution of the parietal and temporal cortex to hand configuration and contextual judgements about tools. Cortex, 49(8), 2097–2105. http://doi.org/10.1016/j.cortex.2012.11.013 CrossRefGoogle ScholarPubMed
Avanzini, P., Abdollahi, R.O., Sartori, I., Caruana, F., Pelliccia, V., Casaceli, G., & Orban, G.A. (2016). Four-dimensional maps of the human somatosensory system. Proceedings of the National Academy of Sciences of the United States of America, 113, E1936–E1943. http://doi.org/10.1073/pnas.1601889113 Google ScholarPubMed
Baldo, J.V., Katseff, S., & Dronkers, N.F. (2012). Brain regions underlying repetition and auditory-verbal short-term memory deficits in aphasia: Evidence from voxel-based lesion symptom mapping. Aphasiology, 26(3-4), 338–354. http://doi.org/10.1080/02687038.2011.602391 CrossRefGoogle ScholarPubMed
Boronat, C.B., Buxbaum, L.J., Coslett, H.B., Tang, K., Saffran, E.M., Kimberg, D.Y., && Detre, J.A. (2005). Distinctions between manipulation and function knowledge of objects: Evidence from functional magnetic resonance imaging. Cognitive Brain Research, 23(2-3), 361–373. http://doi.org/10.1016/j.cogbrainres.2004.11.001 CrossRefGoogle ScholarPubMed
Buccino, G., Vogt, S., Ritzl, A., Fink, G.R., Zilles, K., Freund, H., & Rizzolatti, G. (2004). Neural circuits underlying imitation learning of hand actions: An event-related fMRI Study. Neuron, 42, 323–334. http://doi.org/10.1016/S0896-6273(04)00181-3 CrossRefGoogle ScholarPubMed
Buchsbaum, B.R., & D’Esposito, M. (2009). Repetition suppression and reactivation in auditory-verbal short-term recognition memory. Cerebral Cortex, 19(6), 1474–1485. http://doi.org/10.1093/cercor/bhn186 CrossRefGoogle ScholarPubMed
Buxbaum, L.J. (2001). Ideomotor apraxia: A call to action. Neurocase, 7, 445–448.CrossRefGoogle ScholarPubMed
Buxbaum, L.J., Kyle, K., Grossman, M., & Coslett, H.B. (2007). Left inferior parietal representations for skilled hand-object interactions: Evidence from stroke and corticobasal degeneration. Cortex, 43(3), 411–423. http://doi.org/10.1016/S0010-9452(08)70466-0 CrossRefGoogle ScholarPubMed
Buxbaum, L.J., Shapiro, A.D., & Coslett, H.B. (2014). Critical brain regions for tool-related and imitative actions: A componential analysis. Brain, 137(7), 1971–1985. http://doi.org/10.1093/brain/awu111 CrossRefGoogle ScholarPubMed
Buxbaum, L.J., Sirigu, A., Schwartz, M.F., & Klatzky, R. (2003). Cognitive representations of hand posture in ideomotor apraxia. Neuropsychologia, 41(8), 1091–1113. http://doi.org/10.1016/S0028-3932(02)00314-7 CrossRefGoogle ScholarPubMed
Canessa, N., Borgo, F., Cappa, S.F., Perani, D., Falini, A., Buccino, G., & Shallice, T. (2008). The different neural correlates of action and functional knowledge in semantic memory: An fMRI study. Cerebral Cortex, 18(4), 740–751. http://doi.org/10.1093/cercor/bhm110 CrossRefGoogle ScholarPubMed
Caspers, S., Zilles, K., Laird, A.R., & Eickhoff, S.B. (2010). ALE meta-analysis of action observation and imitation in the human brain. Neuroimage, 50(3), 1148–1167. http://doi.org/10.1016/j.neuroimage.2009.12.112 CrossRefGoogle ScholarPubMed
Chaminade, T., Meltzoff, A.N., & Decety, J. (2005). An fMRI study of imitation: Action representation and body schema. Neuropsychologia, 43(1), 115–127. http://doi.org/10.1016/j.neuropsychologia.2004.04.026 CrossRefGoogle ScholarPubMed
de Lange, F.P., Helmich, R.C., & Toni, I. (2006). Posture influences motor imagery: An fMRI study. Neuroimage, 33(2), 609–617. http://doi.org/10.1016/j.neuroimage.2006.07.017 CrossRefGoogle ScholarPubMed
Decety, J. (1996). Do imagined and executed actions share the same neural substrate? Cognitive Brain Research, 3(2), 87–93. http://doi.org/10.1016/0926-6410(95)00033-X CrossRefGoogle ScholarPubMed
Gelfand, J.R., & Bookheimer, S.Y. (2003). Dissociating neural mechanisms of temporal sequencing and processing phonemes. Neuron, 38(5), 831–842. http://doi.org/10.1016/S0896-6273(03)00285-X CrossRefGoogle ScholarPubMed
Goldenberg, G., & Hagmann, S. (1998). Tool use and mechanical problem solving in apraxia. Neuropsychologia, 36(7), 581–589. http://doi.org/S0028-3932(97)00165-6 [pii] CrossRefGoogle ScholarPubMed
Goldenberg, G., & Spatt, J. (2009). The neural basis of tool use. Brain, 132(6), 1645–1655. http://doi.org/10.1093/brain/awp080 CrossRefGoogle ScholarPubMed
Haaland, K.Y., Harrington, D.L., & Knight, R.T. (2000). Neural representations of skilled movement. Brain, 123, 2306–2313.CrossRefGoogle ScholarPubMed
Hétu, S., Grégoire, M., Saimpont, A., Coll, M.P., Eugène, F., Michon, P.E., && Jackson, P.L. (2013). The neural network of motor imagery: An ALE meta-analysis. Neuroscience and Biobehavioral Reviews, 37(5), 930–949. http://doi.org/10.1016/j.neubiorev.2013.03.017 CrossRefGoogle ScholarPubMed
Humphreys, G.F., & Lambon Ralph, M.A. (2015). Fusion and fission of cognitive functions in the human parietal cortex. Cerebral Cortex, 25, 3547–3560.CrossRefGoogle ScholarPubMed
Ishibashi, R., Lambon Ralph, M.A., Saito, S., & Pobric, G. (2011). Different roles of lateral anterior temporal lobe and inferior parietal lobule in coding function and manipulation tool knowledge: Evidence from an rTMS study. Neuropsychologia, 49(5), 1128–1135. http://doi.org/10.1016/j.neuropsychologia.2011.01.004 CrossRefGoogle ScholarPubMed
Ishibashi, R., Pobric, G., Saito, S., & Lambon Ralph, M.A. (2016). The neural network for tool-related cognition: An activation likelihood estimation meta-analysis of 49 neuroimaging studies. Cognitive Neuropsychology, 33(3-4), 241–256. http://doi.org/10.1080/02643294.2016.1188798 CrossRefGoogle Scholar
Jarry, C., Osiurak, F., Delafuys, D., Chauviré, V., Etcharry-Bouyx, F., & Le Gall, D. (2013). Apraxia of tool use: More evidence for the technical reasoning hypothesis. Cortex, 49(9), 2322–2333. http://doi.org/10.1016/j.cortex.2013.02.011 CrossRefGoogle ScholarPubMed
Jeannerod, M. (1994). The representing brain: Neural correlates of motor intention and imagery. Behavioral and Brain Sciences, 17, 187–245.CrossRefGoogle Scholar
Kalénine, S., Buxbaum, L.J., & Coslett, H.B. (2010). Critical brain regions for action recognition: Lesion symptom mapping in left hemisphere stroke. Brain, 133(11), 3269–3280. http://doi.org/10.1093/brain/awq210 CrossRefGoogle ScholarPubMed
Kraemer, D.J.M., Hamilton, R.H., Messing, S.B., Desantis, J.H., & Thompson-Schill, S.L. (2014). Cognitive style, cortical stimulation, and the conversion hypothesis. Frontiers in Human Neuroscience, 8, 15. http://doi.org/10.3389/fnhum.2014.00015 CrossRefGoogle ScholarPubMed
Lacadie, C.M., Fulbright, R.K., Constable, R.T., & Papademetris, X. (2008). More accurate Talairach coordinates for neuroimaging using nonlinear registration. Neuroimage, 42, 717–725.CrossRefGoogle Scholar
Lesourd, M., Baumard, J., Jarry, C., Etcharry-Bouyx, F., Belliard, S., Moreaud, O., & Osiurak, F. (2017). Rethinking the cognitive mechanisms underlying pantomime of tool use: Evidence from Alzheimer’s disease and semantic dementia. Journal of the International Neuropsychological Society, 23(2), 128–138. http://doi.org/10.1017/S1355617716000618 CrossRefGoogle ScholarPubMed
Lesourd, M., Baumard, J., Jarry, C., Le Gall, D., & Osiurak, F. (2016). A cognitive-based model of tool use in normal aging. Aging, Neuropsychology, and Cognition, 1–24. http://doi.org/10.1080/13825585.2016.1218822 Google ScholarPubMed
Mengotti, P., Corradi-Dell’Acqua, C., Negri, G.A.L., Ukmar, M., Pesavento, V., & Rumiati, R.I. (2013). Selective imitation impairments differentially interact with language processing. Brain, 136(8), 2602–2618. http://doi.org/10.1093/brain/awt194 CrossRefGoogle ScholarPubMed
Niessen, E., Fink, G.R., & Weiss, P.H. (2014). Apraxia, pantomime and the parietal cortex. Neuroimage: Clinical, 5, 42–52. http://doi.org/10.1016/j.nicl.2014.05.017 CrossRefGoogle ScholarPubMed
Oberhuber, M., Hope, T.M.H., Seghier, M.L., Parker Jones, O., Prejawa, S., Green, D.W., && Price, C.J. (2016). Four functionally distinct regions in the left supramarginal gyrus support word processing. Cerebral Cortex, 26(11), 4212–4226. http://doi.org/10.1093/cercor/bhw251 CrossRefGoogle ScholarPubMed
Orban, G.A., & Caruana, F. (2014). The neural basis of human tool use. Frontiers in Psychology, 5, 1–12. http://doi.org/10.3389/fpsyg.2014.00310 CrossRefGoogle ScholarPubMed
Osiurak, F., & Badets, A. (2016). Tool use and affordance: Manipulation-based versus reasoning-based approaches. Psychological Review, 123(2), 534–568. http://doi.org/10.1037/rev0000027 CrossRefGoogle ScholarPubMed
Osiurak, F., Jarry, C., Allain, P., Aubin, G., Etcharry-Bouyx, F., Richard, I., & Le Gall, D. (2009). Unusual use of objects after unilateral brain damage. The technical reasoning model. Cortex, 45(6), 769–783. http://doi.org/10.1016/j.cortex.2008.06.013 Google ScholarPubMed
Osiurak, F., Jarry, C., & Le Gall, D. (2010). Grasping the affordances, understanding the reasoning: Toward a dialectical theory of human tool use. Psychological Review, 117(2), 517–540. http://doi.org/10.1037/a0019004 CrossRefGoogle Scholar
Osiurak, F., Jarry, C., & Le Gall, D. (2011). Re-examining the gesture engram hypothesis. New perspectives on apraxia of tool use. Neuropsychologia, 49(3), 299–312. http://doi.org/10.1016/j.neuropsychologia.2010.12.041 Google ScholarPubMed
Osiurak, F., Jarry, C., Lesourd, M., Baumard, J., & Le Gall, D. (2013). Mechanical problem-solving strategies in left-brain damaged patients and apraxia of tool use. Neuropsychologia, 51(10), 1964–1972. http://doi.org/10.1016/j.neuropsychologia.2013.06.017 CrossRefGoogle ScholarPubMed
Osiurak, F., & Lesourd, M. (2014). What about mechanical knowledge? Physics of Life Reviews, 11(2), 269–270. http://doi.org/10.1016/j.plrev.2014.01.013 CrossRefGoogle ScholarPubMed
Parsons, L.M. (1994). Temporal and kinematic properties of motor behavior reflected in mentally simulated action. Journal of Experimental Psychology. Human Perception and Performance, 20(4), 709–730. http://doi.org/10.1037/0096-1523.20.4.709 CrossRefGoogle ScholarPubMed
Peeters, R.R., Rizzolatti, G., & Orban, G.A. (2013). Functional properties of the left parietal tool use region. Neuroimage, 78, 83–93. http://doi.org/10.1016/j.neuroimage.2013.04.023 CrossRefGoogle ScholarPubMed
Pelgrims, B., Andres, M., & Olivier, E. (2009). Double dissociation between motor and visual imagery in the posterior parietal cortex. Cerebral Cortex, 19(10), 2298–2307. http://doi.org/10.1093/cercor/bhn248 CrossRefGoogle ScholarPubMed
Pelgrims, B., Olivier, E., & Andres, M. (2011). Dissociation between manipulation and conceptual knowledge of object use in the supramarginalis gyrus. Human Brain Mapping, 32(11), 1802–1810. http://doi.org/10.1002/hbm.21149 CrossRefGoogle ScholarPubMed
Przybylski, Ł., & Króliczak, G. (2017). Planning functional grasps of simple tools invokes the hand-independent praxis representation network: An fMRI study. Journal of the International Neuropsychological Society, 23(2), 108–120. http://doi.org/10.1017/S1355617716001120 CrossRefGoogle ScholarPubMed
Reynaud, E., Lesourd, M., Navarro, J., & Osiurak, F. (2016). On the neurocognitive origins of human tool use a critical review of neuroimaging data. Neuroscience & Biobehavioral Reviews, 64, 421–437. http://doi.org/10.1016/j.neubiorev.2016.03.009 CrossRefGoogle ScholarPubMed
Rothi, L.J.G., Ochipa, C., & Heilman, K.M. (1991). A cognitive neuropsychological model of limb praxis. Cognitive Neuropsychology, 8(6), 443–458. http://doi.org/10.1080/02643299108253382 CrossRefGoogle Scholar
Thielscher, A., & Kammer, T. (2002). Linking physics with physiology in TMS: A sphere field model to determine the cortical stimulation site in TMS. Neuroimage, 17(3), 1117–1130. http://doi.org/10.1006/nimg.2002.1282 CrossRefGoogle ScholarPubMed
Toschi, N., Welt, T., Guerrisi, M., & Keck, M.E. (2008). A reconstruction of the conductive phenomena elicited by transcranial magnetic stimulation in heterogeneous brain tissue. Physica Medica, 24(2), 80–86. http://doi.org/10.1016/j.ejmp.2008.01.005 CrossRefGoogle ScholarPubMed
Van Elk, M. (2014). The left inferior parietal lobe represents stored hand-postures for object use and action prediction. Frontiers in Psychology, 5, 1–12. http://doi.org/10.3389/fpsyg.2014.00333 CrossRefGoogle ScholarPubMed
Van Essen, D.C. (2005). A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. Neuroimage, 28(3), 635–662. http://doi.org/10.1016/j.neuroimage.2005.06.058 CrossRefGoogle ScholarPubMed
Van Essen, D.C., Drury, H.A., Dickson, J., Harwell, J., Hanlon, D., & Anderson, C.H. (2001). An integrated software suite for surface-based analyses of cerebral cortex. Journal of the American Medical Informatics Association, 8(5), 443–459. http://doi.org/10.1136/jamia.2001.0080443 CrossRefGoogle ScholarPubMed